Progress Toward Measles Elimination in the Eastern Mediterranean Region

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1 SUPPLEMENT ARTICLE Progress Toward Measles Elimination in the Eastern Mediterranean Region Boubker Naouri, 1 Hinda Ahmed, 1 Raef Bekhit, 1 Nadia Teleb, 1 Ezzeddine Mohsni, 2 and James P. Alexander Jr. 3 1 Vaccine Preventable Diseases and Immunization and 2 Disease Surveillance, Eradication and Elimination, Regional Office for the Eastern Mediterranean, World Health Organization, Cairo, Egypt; and 3 Global Immunization Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia Since 1997, when the goal of interrupting measles transmission by 2010 was adopted, substantial progress has been made toward the elimination of measles in the Eastern Mediterranean Region (EMR). For the 22 EMR member countries, routine coverage with the first dose of a measles-containing vaccine (MCV) increased from 70% in 1997 to 82% in All 22 countries conducted measles catch-up vaccination campaigns during , and most conducted follow-up campaigns as needed. Of the 22 EMR countries, 19 have established case-based surveillance for measles with laboratory confirmation. Reported measles cases decreased by 86% during , and estimated measles mortality decreased by 93% during , accounting for 17% of global measles mortality reduction during that period. Despite these successes, several significant challenges remain, and the EMR will not be able to achieve measles elimination by the end of Achieving and maintaining high population immunity with 2 doses of MCV, improving sensitive case-based surveillance, identifying and vaccinating high-risk subpopulation groups, and appropriately responding to outbreaks are key steps needed to achieve the goal. The Eastern Mediterranean Region (EMR) of the World Health Organization (WHO) includes 22 countries that stretch from Morocco in the west to Pakistan in the east and are home to.550 million people (for this report, the geographic regions West Bank and Gaza Strip are considered to constitute 1 of the 22 countries of the region). There is a wide variation in the gross national product (GNP) per capita among the countries of the region, ranging from a low of US$ 160 for Afghanistan to a high of US$ 28,270 for Qatar. Five countries (Afghanistan, Djibouti, Somalia, Sudan, and Yemen) are among the least developed countries in the world [1]. The geopolitical situation of the Region is complex: Potential conflicts of interest: none reported. Supplement sponsorship: This article is part of a supplement entitled "Global Progress Toward Measles Eradication and Prevention of Rubella and Congenital Rubella Syndrome," which was sponsored by the Centers for Disease Control and Prevention. Correspondence: James P. Alexander, Jr, MD, Centers for Disease Control and Prevention, 1600 Clifton Rd, NE, Mailstop E-05, Atlanta, Georgia (axj1@cdc.gov). The Journal of Infectious Diseases 2011;204:S289 S298 Published by Oxford University Press on behalf of the Infectious Diseases Society of America (print)/ (online)/2011/204s1-0037$14.00 DOI: /infdis/jir140 several countries are in a state of crisis and conflict or have experienced natural disasters, including Afghanistan, Iraq, Pakistan, West Bank and Gaza Strip, Somalia, Sudan and Yemen. Providing emergency medical assistance and technical support to these countries has been a challenging undertaking for the WHO Regional Office for the Eastern Mediterranean (EMRO). In 1997, the 22 EMR member countries resolved to eliminate measles from the region by 2010, defined as the absence of endemic measles cases in a defined geographical area for.12 months in the presence of a wellperforming surveillance system. (One measure suggesting measles elimination is a sustained measles incidence of,1 case per 1 million population confirmed by laboratory or epidemiological linkage [excluding clinically compatible and imported cases].) Key strategies for achieving measles elimination in the region included (1) achieving and maintaining R90% vaccination coverage of children with the first dose of measles-containing vaccine (MCV1) in every district of each country through routine immunization services, (2) achieving R90% vaccination coverage with a second dose of a measles-containing vaccine (MCV2) in every district either through a routine 2-dose vaccination schedule or through supplemental immunization activities (SIAs), Measles Elimination Progress Eastern Mediterranean Region d JID 2011:204 (Suppl 1) d S289

2 (3) establishing high-quality case-based surveillance with investigation and laboratory testing in a proficient measles laboratory of all suspected cases of measles, and (4) providing optimal clinical-case management, including supplementation of diets with vitamin A [2]. In 1999, the EMRO developed a 5- year plan for measles elimination based on the joint WHO United Nations Children s Fund (UNICEF) strategy for measles mortality reduction. A second plan was developed for the period [3]. Significant progress has been made in the EMR toward measles elimination, through increasing coverage with a routine MCV1 and implementation of catch-up and follow-up measles SIAs in EMR countries. The number of confirmed measles cases has decreased dramatically from 89,518 in 1998 to 12,186 in 2008 (86% decrease), and the EMR achieved a 93% reduction in estimated measles mortality during the largest percentage reduction among all WHO regions, accounting for 17% of the global reduction in measles mortality [4]. Despite these successes, in recent years, there has been a resurgence of measles virus circulation and outbreaks in a number of countries, including a nationwide epidemic in Iraq during Although several countries are near elimination, the EMR as a whole will not reach the goal of measles elimination by 2010, based on current levels of measles control. In this article, we summarize the impact of measles elimination strategies on the interruption of measles transmission in the EMR during the period and the challenges that remain to reach the goal. METHODS Vaccination Strategy and Coverage On the basis of WHO recommendations, MCV1 has been administered in the EMR to children at 9 months of age in countries with high measles incidence and to children 12 months of age in countries with low measles incidence and a low risk of measles infection among infants [5]. To interrupt the transmission of measles, EMRO recommended in 1997 that all countries conduct an initial SIA (catch-up campaign) against measles, targeting all children 9 months 14 years of age and to add MCV2 to the routine immunization schedule in those countries that achieved.80% MCV1 coverage for 3 years consecutively. On the basis of the experience in the Americas, EMRO recommended that countries unable to meet this criterion continue to increase MCV1 coverage and conduct additional measles SIAs (follow-up campaigns) at appropriate intervals, usually every 2 4 years [6]. As of 2009, MCV1 is administered at age 9 months in 8 (36%) of the EMR countries and at age months in the remaining 14 (64%) countries (Table 1). Nineteen (86%) countries have a routine 2-dose measles vaccination schedule; MCV2 is administered at months, months, and 4 6 years in 1 (5%), 9 (47%), and 9 (47%) of the 2-dose countries, respectively. Twelve (55%) countries in the region use a combined measles, mumps and rubella (MMR) vaccine for MCV1, and 14 (64%) use MMR for MCV2. Five countries have a 3-dose measles vaccine schedule, including a dose of monovalent measles vaccine at 9 months, because of either recent outbreaks affecting infants or transition from a 9-month to a 12-month MCV1 schedule. Vaccination coverage with MCV1 and MCV2 is calculated annually for each country by dividing the total number of doses administered to children in the targeted age group by the estimated population of children in that age group based on the most recent census (the administrative method). In addition, the WHO and UNICEF estimate coverage of MCV1 annually for each country using reported coverage of MCV1, survey results, and other information [7]. The 22 EMR countries conducted measles or combined measles-rubella SIAs during , the last of which occurred in Iraq in December 2009 (Table 2). All countries conducted catch-up SIAs, generally targeting children aged 9 months 14 years, to rapidly interrupt measles transmission. Many countries conducted R1 follow-up measles SIAs, generally targeting children aged 9 59 months, to prevent the buildup of susceptible children and reduce the risk of outbreaks. As needed, countries conducted smaller-scale, focused immunization campaigns in high-risk areas, often in response to measles case-clusters, or larger-scale campaigns in response to outbreaks [8]. Vaccination coverage for SIAs is calculated by dividing the total number of doses administered to children in the targeted age group by the estimated population of children in that age group. Some countries also conducted vaccination coverage surveys to independently assess the coverage of SIAs. Disease Surveillance After completion of initial catch-up campaigns, measles surveillance was intensified in all countries in the EMR. Since 2006, 19 (86%) 22 countries in the region have conducted case-based surveillance (CBS). Of the 3 countries without CBS, Morocco and Pakistan have sentinel surveillance for measles with laboratory confirmation of cases identified at sentinel sites, and Somalia is initiating sentinel site surveillance for measles. Standard WHO definitions are used for surveillance; confirmation of measles is made by clinical diagnosis, epidemiologic linking, or laboratory testing [9]. In countries with CBS, a thorough investigation of each suspected measles case is done, with collection of clinical and epidemiologic data on an individual case-reporting form, collection of serum for detection of measles-specific immunoglobulin M (IgM) antibodies, and collection of serum or other specimens for virus isolation [10]. By 2006, all countries were reporting measles and rubella data to EMRO on a monthly basis, and all countries have demonstrated significant improvement in management and sharing of measles surveillance and laboratory data during the past few years. In the S290 d JID 2011:204 (Suppl 1) d Naouri et al

3 Table 1. Recommended 2009 Routine Measles Vaccine a Schedules and Percentage of Children Who Received Their First Dose of Measles Vaccine b, by Country/Area World Health Organization (WHO) Eastern Mediterranean Region, Coverage, % Country/Area Age at first dose Age at second dose Afghanistan 9 mos c 18 mos c d Bahrain 12 mos 5 yrs Djibouti 9 mos c None d Egypt 12 mos 18 mos Iran 12 mos 18 mos Iraq e 15 mos c 4-6 yrs d Jordan e 12 mos 18 mos Kuwait 12 mos 4-6 yrs Lebanon e 12 mos 4-6 yrs d Libya 12 mos 18 mos Morocco 9 mos c 6 yrs c Oman 12 mos 18 mos Pakistan 9 mos c mos c d West Bank and Gaza Strip 12 mos 18 mos Qatar 12 mos 4-6 yrs Saudi Arabia e 12 mos 4-6 yrs Somalia 9 mos c None d Sudan f 9 mos c None d Syria 12 mos 18 mos d Tunisia 15 mos c 6 yrs c United Arab Emirates e 15 mos 6 yrs Yemen 9 mos c 18 mos c d Region overall d NOTE. a A combined measles, mumps and rubella (MMR) vaccine is used except where noted. b By age 12 months or later if first dose was scheduled after age 12 months. Data are from WHO and United Nations Children Fund (UNICEF) estimates. c Single-antigen measles vaccine used, except Morocco, where 2nd dose vaccine is a combined measles-rubella vaccine. d Vaccination coverage was below the regional goal of 90% in e Country has a 3-dose measles vaccination schedule, including a dose of monovalent measles vaccine given at 9 months of age. f Includes partial data for Southern Sudan. absence of a routine surveillance system for measles-related deaths, the WHO uses a model to estimate measles-associated mortality based on measles case counts (corrected for a certain level of underreporting), estimated case-fatality rates, and estimated vaccination coverage [11]. In 2006, the WHO s Technical Advisory Group on Immunization in the EMR recommended monitoring surveillance performance, using standard indicators and targets. These standards include ensuring that (1) R 2 non-measles suspected measles cases per 100,000 persons are detected and reported (to monitor the sensitivity of the surveillance system), (2) R80% of suspected cases have adequate investigation (ie, investigation conducted within 48 h after notification that includes all essential data elements), (3) R80% of suspected measles cases are tested for measles IgM antibody (to monitor adequacy of testing), (4) R80% of specimens are received by a laboratory within 7 days after collection (to monitor timeliness of specimen transportation), (5) R80% of specimens sent to the laboratory arrive in good condition (to monitor adequacy of specimen collection), and (6) R80% of laboratory test results are reported within 7 days after receipt in the laboratory (to monitor timely reporting). Rubella surveillance is integrated with measles surveillance, because most countries use the febrile rash illness definition for suspect measles cases and perform laboratory testing for both measles-specific and rubella-specific IgM antibodies. Laboratory Surveillance The EMR Measles and Rubella Laboratory Network (LabNet) was initiated in 2002 to support measles and rubella surveillance, and it became fully functional in all EMR countries in The LabNet is composed of 22 national laboratories and 2 Regional Reference Laboratories (RRLs), one each in Oman and Tunisia. EMRO provides funding support to ensure that the LabNet has adequate supplies and equipment. National laboratories perform confirmatory testing of serum specimens from suspected measles cases using validated enzymelinked immunosorbent assays (ELISAs) to detect measles immunoglobulin M (IgM) antibodies and, if negative, to test for Measles Elimination Progress Eastern Mediterranean Region d JID 2011:204 (Suppl 1) d S291

4 Table 2. Measles Supplementary Immunization Activities (SIAs), by Country/Area, Target Age Group, Type of SIA, and Number and Percentage of Targeted Children Vaccinated World Health Organization (WHO) Eastern Mediterranean Region, No. and % of targeted children vaccinated Country/Area Year Target age group Type of SIA No. % a Afghanistan mos High-risk area 74, mos 14 yrs Catch-up 8,791, mos Follow-up 5,338, mos Follow-up phase 1 1,064, mos Follow-up phase 2 1,809, mos Follow-up phase 3 2,085, mos Follow-up phase 1 702, mos Follow-up phase 2 1,652, mos Follow-up phase 3 646, Bahrain yrs Catch-up phase 1 127, yrs Catch-up phase 2 63, Djbouti mos Follow-up 72, mos Follow-up 77, mos 15 yrs Catch-up 186, mos High-risk area 7, mos 15 yrs Catch-up 184, Egypt mos High-risk area 1,864, yrs Catch-up phase 1 5,616, yrs Catch-up phase 2 3,220, yrs Catch-up phase 1 18,375, yrs Catch-up phase 2 17,843, Iran mos 14 yrs High-risk area 6,518, yrs Catch-up 33,527, yrs Follow-up 310, Iraq mos High-risk area 2,388, mos Catch-up phase 1 3,619, yrs Catch-up phase 2 5,123, yrs Catch-up 862, mos 7 yrs High-risk area 37, mos Follow-up 2,650, mos Follow-up 900, mos High-risk area 43, mos Follow-up 3,560, mos High-risk area 198, mos High-risk area 52, mos High-risk area 38, mos High-risk area 154, mos Follow-up 659, mos 12 yrs Follow-up 10,965, Jordan yrs Catch-up 1,090, yrs Catch-up 251, mos 14 yrs High-risk area 3, yrs Catch-up 175, Kuwait yrs Catch-up 295, yrs Follow-up 154, yrs High-risk area 38, Lebanon yrs Catch-up 1,059, mos 15 yrs Catch-up 705, Libya mos 20 yrs Catch-up 2,695, mos Follow-up 748, S292 d JID 2011:204 (Suppl 1) d Naouri et al

5 Table 2. (Continued) No. and % of targeted children vaccinated Country/Area Year Target age group Type of SIA No. % a Morocco mos 14 yrs Catch-up 4,665, Oman mos 18 yrs Catch-up 705, Pakistan mos High-risk area 1,232, mos 15 yrs Catch-up phase 1 2,511, mos 13 yrs Catch-up phase 2 1,282, mos 13 yrs Catch-up phase 3 6,906, mos 13 yrs Catch-up phase 4 20,566, mos 13 yrs Catch-up phase 5 35,315, West Bank and Gaza yrs High-risk area 17, yrs Catch-up 415, Qatar yrs Catch-up 80, mos 15 yrs Catch-up 319, mos Follow-up 32, Saudi Arabia yrs Catch-up phase 1 1,629, yrs Catch-up phase 2 3,179, yrs Follow-up 1,079, mos 18 yrs Catch-up 6,886, Somalia mos 15 yrs Catch-up phase 1 319, mos 15 yrs Catch-up phase 2 2,019, mos 15 yrs Catch-up phase 3 2,774, mos Follow-up phase 1 b 250, mos Follow-up phase 1 b 352, mos Follow-up phase 1 b 214, mos Follow-up phase 1 b 119, mos Follow-up phase 2 b 276, mos Follow-up phase 2 b 137, mos Follow-up phase 2 b 517, Sudan mos 15 yrs High-risk area 115, mos 15 yrs High-risk area 980, mos 15 yrs Catch-up phase 1 1,438, mos 15 yrs Catch-up phase 2 2,687, mos 15 yrs Catch-up phase 3 4,020, mos 15 yrs Catch-up phase 4 2,503, mos 5 yrs Follow-up phase 1 1,491, mos 5 yrs Follow-up phase 2 2,728, Southern Sudan mos 14 yrs Catch-up 1,495, mos 14 yrs Catch-up 385, mos 14 yrs Catch-up phase 1 362, mos 14 yrs Catch-up phase 2 1,514, mos 14 yrs Catch-up phase 3 1,698, mos 14 yrs Catch-up phase 4 132, Syria mos 15 yrs Catch-up 6,636, yrs High-risk area 324, mos 7 yrs Catch-up phase 1 3,172, yrs Catch-up phase 2 1,610, yrs Catch-up phase 3 1,610, Tunisia yrs Catch-up 1,754, mos 5 yrs Follow-up 514, mos 5 yrs Follow-up 126, yrs Catch-up 562, Measles Elimination Progress Eastern Mediterranean Region d JID 2011:204 (Suppl 1) d S293

6 Table 2. (Continued) No. and % of targeted children vaccinated Country/Area Year Target age group Type of SIA No. % a United Arab Emirates mos Catch-up phase 1 154, yrs Catch-up phase 2 168, mos 18 yrs Catch-up 893, Yemen mos Catch-up 2,205, mos High-risk area 116, mos 15 yrs Catch-up 9,322, mos 15 yrs High-risk area 1,291, mos High-risk area 621, mos Follow-up 3,246, All countries 298,325,513 NOTE. a The percentage of the population vaccinated may exceed 100% because of underestimation of the size of the target population. b Follow-up campaign conducted as part of Child Health Days, a campaign to deliver multiple vaccinations and interventions to infants, children and women of child-bearing age. rubella IgM antibodies. Participating laboratories are required to report results to the Expanded Program on Immunization (EPI) within 7 days after receipt of specimen in the laboratory. Staff in all 22 national laboratories have been trained in measles and rubella serological testing, participate in global annual proficiency panel testing, and undergo periodic accreditation using a WHO standardized checklist, to review their performance activities, timeliness, and quality indicators. To improve virologic surveillance, 17 (77%) of the 22 national laboratories received training during in virus detection and molecular characterization. All 17 now have the capacity to do measles and rubella virus isolation or reverse-transcriptionpolymerase chain reaction (RT-PCR) testing. The 2 national laboratories selected to serve as RRLs function as specialized diagnostic laboratories, performing virus isolation, virus detection by RT-PCR, and virus sequencing and genotyping. They also provide quality control by validating IgM tests of the national laboratories and build capacity of the LabNet through training courses. RESULTS Vaccination Coverage For the region overall, the estimated routine MCV1 coverage increased from 67% in 1990 to 82% in 2009 (Figure 1). During , routine MCV1 coverage was high and stable or increased in 17 (77%) countries and was low or decreased in 5 (23%) countries (Table 1). In 2009, 4 (18%) countries had MCV1 coverage,70% (range, 24% 69%), 5 (23%) countries had MCV1 coverage of 70% 89%; and 13 (59%) countries achieved a coverage of.90%. Of these 13 countries, 11 reported.90% MCV1 coverage in all districts. In the 19 countries with a routine 2-dose schedule, 12 (63%) reported MCV2 coverage.90% nationally in During , nearly 300 million children in the EMR were vaccinated through SIAs (Table 2). The largest campaigns were conducted in Iran (33,527,337 persons 5-25 years vaccinated in 2003), Pakistan (66,582,317 children aged 9 months 14 years vaccinated in ), Egypt (36,218,900 persons 2-20 years vaccinated during ), and Iraq (10,965,289 children 6 months 12 years old vaccinated in 2009). Six countries (Djibouti, Egypt, Lebanon, Saudi Arabia, Syria, and Tunisia) conducted repeat catch-up campaigns, either to achieve better immunity in the target population or because timely follow-up SIAs were not conducted and large measles outbreaks occurred. Vaccination coverage during initial catch-up campaigns, based on doses administered, was 69% 105% and, during all measles SIAs, was 37% 118%. Disease Surveillance Before introduction of measles vaccination in the early 1980s, 200,000 clinically diagnosed cases of measles were reported each year in EMR countries [12]. After strengthening measlescontrol activities throughout the 1980s, reported cases decreased by 70% to 59,058 in 1990, and measles epidemics became smaller in size and the interval between them increased from 2 4 years during to 5 6 years during (Figure 1) [13]. Since setting the elimination goal, measles cases in the EMR decreased from 89,518 in 1998 to 12,186 in 2008, an 86% decrease, with a resulting decrease in the measles incidence rate from 188 to 21 confirmed measles cases per 1 million persons during , respectively (Figure 1). Six countries have reported measles incidence,1 case per million persons in the presence of a sensitive and well-functioning surveillance system: Bahrain, Iran, Jordan, West Bank and Gaza Strip, Syria, and Tunisia. Estimated measles mortality in the EMR decreased from 101,000 in 2000 to 7000 in 2008, a 93% decrease [4]. Despite the overall reduction in the number of confirmed measles cases, a number of countries in the region experienced S294 d JID 2011:204 (Suppl 1) d Naouri et al

7 Figure 1. Number of reported measles cases a and estimated percentage of children who received their first dose of measles vaccine b World Health Organization (WHO) Eastern Mediterranean Region, a Confirmed cases of measles reported to WHO and the United Nations Children's Fund (UNICEF) through the Joint Reporting Form Regional Office for the Eastern Mediterranean Region. b By age 12 months or later if the first dose was scheduled after age of 12 months. Data are from WHO and UNICEF estimates. c This goal, to reduce measles mortality by 50% from 1999 to 2005, has been achieved. d This goal is to reduce measles mortality by 90% from 2006 to large-scale measles outbreaks during Despite the reported MCV1 coverage rates of.95%, a routine 2-dose schedule, and a catch-up SIA held during the preceding 8 years, measles outbreaks occurred in Lebanon (1947 cases; ), Syria (1295 cases; ), Qatar (505 cases; ), Saudi Arabia (5455 cases; ), and Egypt (3305 cases; ). Large outbreaks also occurred in countries with a higher burden of measles because of incomplete implementation of elimination strategies or conflict and insecurity, including Morocco (4920 cases; ), Somalia (2230 cases; ), Afghanistan (4460 cases; ), and Iraq (35,822 cases; ). The number of confirmed cases of measles reported to EMRO increased from 12,186 in 2008 to 36,737 in 2009, largely because of 30,328 confirmed cases in Iraq in 2009 (Of the 30,328 confirmed measles cases reported by Iraq in 2009, 8753 had detailed case investigations with collection of serum specimen for laboratory testing, whereas 21,570 were clinical cases of measles with epidemiologic linkage to confirmed cases). Of the 15,866 confirmed measles cases with individual case information reported to EM- RO in 2009 (including 8753 of 30,328 cases in Iraq), 53% were male and 47% were female; 17% were,1 year of age, 40% were 1 4 years of age, 20% were 5 14 years of age, and 22% were.15 years of age. During 2009, 48% of these confirmed measles cases were unvaccinated. Of those who were vaccinated, 76% and 24% were vaccinated with 1 dose and.2 doses of MCV, respectively. During 2009, among the 19 countries conducting case-based surveillance, the suspected measles case reporting rate for the EMR was 2.19 cases per 100,000 persons. Nine (47%) of the 19 countries achieved the target reporting rate of R2 cases per 100,000 persons. Among the 19 countries, 8 (42%) achieved the target of R80% timely and complete case investigations, 16 (84%) achieved the target of R80% suspected cases tested for measles IgM antibody, and 13 (68%), 18 (95%), and 18 (95%) reached the R 80% targets for timely specimen transportation, adequate specimen collection, and prompt reporting of measles IgM test results, respectively. Three countries met all surveillance quality targets. Laboratory Surveillance Since 2006, all countries have reported measles and rubella laboratory data to EMRO on a monthly basis. Serological testing for measles IgM has increased by 51% in the LabNet, from 6684 to 13,222 serum samples tested in 2006 and 2009, respectively (Table 3). The EMR LabNet has maintained its performance since 2006, obtaining scores.90% on the global annual proficiency tests in all countries. All 22 national laboratories have undergone accreditation reviews, and 20 have passed by fulfilling accreditation criteria. During , only a few EMR countries were conducting virologic surveillance for measles [14, 15]. As a result of training in virus detection and characterization during , 17 (77%) of the 22 countries have now identified R1 measles genotypes (B3, C2,, D5, D6, D7, D8, and H1), and all countries except one have submitted their measles genotypes to the WHO genotype database (Table 4). The predominant genotype in the EMR is, detected in 12 (71%) of 17 countries with identified genotypes; the second most frequently identified is B3, detected in 7 (41%) of these countries. In addition, multiple genotypes have been identified in some countries, such as Oman (D5 and D8 associated with endemic transmission and Measles Elimination Progress Eastern Mediterranean Region d JID 2011:204 (Suppl 1) d S295

8 Table 3. Suspected Measles Cases, Serum Samples Tested for Measles and Rubella Immunoglobulin M (IgM) Antibodies, and Positive IgM Tests for Measles and Rubella WHO Eastern Mediterranean Region, Year Suspected measles cases Samples tested Measles IgM1 Rubella IgM ,070 6,636 1, ,388 7,317 2, ,282 16,054 4,872 1, ,765 10,569 4, ,812 13,222 4, Total 104,317 53,798 17,427 3,894 B3 and associated with importations) and Morocco (B3, C2,, D7, and D8, with C2 the most frequently identified and probable endemic strain) [16]. DISCUSSION Substantial progress has been made toward measles elimination in the EMR. The global goal of 90% reduction in measlesassociated mortality by 2010 was achieved in the region by Similarly, there was an 86% decrease in the number of confirmed measles cases reported during , despite intensification of surveillance and case detection during this period. These reductions were the result of full implementation of the recommended regional measles elimination strategies by several countries and the result of efforts by all countries to increase population immunity to measles and to develop sensitive surveillance and timely response for measles cases and outbreaks. These efforts were aided by a high political commitment at national and regional levels to accelerate measles elimination in the EMR. EMR member countries have increased population immunity and reduced the burden of measles through 2 main strategies. Most countries have increased or maintained a high routine MCV1 coverage during the elimination phase. All countries have also provided a second dose of measles vaccine to all children, either through introduction of MCV2 into the routine immunization program or by conducting catch-up measles SIAs during Many countries have also conducted periodic follow-up campaigns to prevent the build-up of susceptible persons in the population. Table 4. Measles Genotypes Identified in the WHO Eastern Mediterranean Region and Reported to the WHO Genotype Database, Country Genotype associated with endemic transmission Genotype associated with importation Afghanistan Bahrain Djibouti B3 a Egypt Iran H1 Iraq Jordan Kuwait B3, D5, D8 Lebanon Libya B3 Morocco C2 (interrupted), D8 Oman D8, D5 B3, Pakistan West Bank & Gaza Strip Qatar Saudi Arabia Somalia Sudan B3, Syria Tunisia B3 United Arab Emirates Yemen B3 NOTE. a Not yet reported to WHO Genotype data base S296 d JID 2011:204 (Suppl 1) d Naouri et al

9 In addition, enhanced measles surveillance has been successfully implemented throughout the region, including the laboratory investigation of suspected measles cases. By 2009, 19 (86%) countries had instituted nationwide measles case-based surveillance (CBS). The sensitivity of measles surveillance in the region is increasing, timeliness and completeness of investigations are improving, most cases investigated have serum specimens obtained for laboratory testing, and most specimens are being sent to national laboratories promptly and in good condition. The EMR LabNet has made considerable progress since the period in support of measles and rubella surveillance, by expanding and establishing a national measles and rubella laboratory in all countries in the region with full serologic testing capability. Laboratories are functioning at a high level of proficiency, handling an increasing volume of specimens, and providing critical information on both measles and rubella cases. They meet performance indicators for measles case-based surveillance, including timeliness of reporting laboratory test results to the national EPI program and EMRO. During the past 3 years, the LabNet has increased its capacity in molecular techniques, quality control standards, and analysis and validation of results. In consequence, substantial progress has been made in identifying circulating measles genotypes in 17 EMR countries. Nonetheless, the region will not achieve a sustained measles incidence of,1 case per million population by the end of The number of measles cases and disease incidence decreased significantly from 1998 through 2008, but remains well above the elimination threshold. A number of countries have experienced outbreaks, both those with resource constraints and security challenges and also those with good resources and generally highquality immunization programs. Iraq, in particular, experienced a large-scale outbreak during , accounting for.80% of the total regional measles cases in 2009, that resulted, in part, from decreasing population immunity over 5 6 years because of conflict and insecurity in most areas of the country. The EMR still faces several challenges to achieve measles elimination, including increasing population immunity to measles. Routine MCV1 coverage (82%) is still too low to achieve elimination, and although numerous SIAs have been conducted during the last 15 years, vaccination coverage has been variable and might have been overestimated for some campaigns. In some cases, follow-up SIAs were not done in a timely manner, and outbreaks occurred before population immunity could be boosted. In other instances, outbreaks have occurred in high-risk subpopulations, such as nomadic groups or communities bordering neighboring countries where measles is endemic or epidemic, despite overall high population immunity. Countries have been most successful when they have conducted high-quality campaigns and achieved high coverage with routine MCV1 and MCV2 doses. In addition, measles surveillance is still suboptimal in some EMR member countries and areas.in Pakistan and Morocco, measles and rubella surveillance is conducted through sentinel surveillance. In Somalia and southern Sudan, measles surveillance is largely aggregate reporting, and the number of reported measles cases underestimates the true incidence of measles because many persons cannot seek medical attention and reporting of identified cases is incomplete at each level of the reporting system. Some countries or areas in the EMR where the burden of measles remains high (notably Afghanistan, Iraq, Pakistan, Somalia, and southern Sudan) have major challenges in establishing comprehensive measles elimination activities because of competing public health priorities, natural disasters, or civil unrest. Armed conflict and war present major challenges for measles elimination in several areas. Unpredictable mass population movements and resettlements complicate the delivery of routine immunization services and planning of SIAs. Conducting SIAs in conflict settings and in areas with no local government requires establishing close linkages with the local community, establishing days of tranquility for vaccination activities during SIAs, and other special efforts to reach the target population. Even with these efforts, vaccination coverage during SIAs is often suboptimal. High-quality follow-up campaigns are needed in these countries to reduce the number of susceptible persons. Such campaigns will require considerable resources that usually must be provided by donors outside the country. To achieve elimination of measles in the EMR, a number of activities will need to be developed or enhanced to fully implement the 4 strategies. First, member countries with low MCV1 coverage need to enhance their routine immunization programs to improve first-dose coverage as a foundation for population immunity. Second, it may be necessary for many, if not all, member countries to conduct follow-up SIAs every 3 4 years until elimination is achieved. Third, increased efforts are needed in both stable and conflict-affected member countries to target and reach high-risk populations (refugees, internally displaced persons, migrant workers and nomadic groups) with MCV1 and MCV2. Fourth, in-depth reviews of immunization services, including independent surveys of vaccination coverage and assessment of data quality, are needed to identify and correct programmatic shortfalls in those countries with high coverage of MCV1, a routine 2-dose schedule, and recently implemented SIAs that have experienced periodic outbreaks. Fifth, there is a need for increased communication and coordination between member countries and EMRO to improve surveillance, epidemiological analysis,andoutbreakresponse.last, continued technical and financial support to low-income countries will be needed to interrupt measles transmission and prevent outbreaks. Achieving, maintaining, and certifying measles elimination in the EMR will be challenging and will require extensive surveillance and monitoring of performance. Laboratorybased surveillance for measles is a cornerstone of the Measles Elimination Progress Eastern Mediterranean Region d JID 2011:204 (Suppl 1) d S297

10 elimination strategy to confirm measles infection in persons with suspect measles and to determine whether identified measles virus is indigenous or imported. Although considerable progress has been made in improving measles virologic surveillance, further efforts are needed to enhance molecular epidemiologic surveillance to document viral transmission pathways and confirm the interruption of endemic measles virus circulation in the EMR. Funding This work was supported by the World Health Organization (to B. N., H. A., N. T., E. M., and R. B.) and Centers for Disease Control and Prevention (Dr Alexander). Acknowledgments We thank the ministries of health of Afghanistan, Bahrain, Djibouti, Egypt, Iran, Iraq, Jordan, Kuwait, Lebanon, Libya, Morocco, Oman, Pakistan, West Bank and Gaza Strip, Qatar, Saudi Arabia, Somalia, Sudan, Syria, Tunisia, United Arab Emirates, and Yemen and the health authorities of the Palestinian populations served by the United Nations Relief Works Agency. References 1. United Nations Conference on Trade and Development. UN Recognition of the least developed countries. Accessed 22 November World Health Organization. Measles: regional strategy for measles elimination. htm. Accessed 22 November World Health Organization. Measles elimination and prevention of congenital rubella syndrome in the Eastern Mediterranean Region. Accessed 22 November World Health Organization. Global reductions in measles mortality and the risk of measles resurgence. Wkly Epidemiol Rec 2009; 84: World Health Organization. Measles vaccines: WHO position paper. Wkly Epidemiol Rec 2009; 84: De Quadros CA, Olive JM, Hersh BS, et al. Measles elimination in the Americas-evolving strategies. JAMA 1996; 275: WHO/UNICEF estimates of national immunization coverage, immunization_coverage/en/index4.html. Accessed 23 November World Health Organization. Response to measles outbreak in measles mortality reduction settings. IVB_09.03_eng.pdf. Accessed 23 November World Health Organization. Monitoring progress towards measles elimination. Wkly Epidemiol Rec 2010; 49: CDC. Measles, mumps and rubella-vaccine use and strategies for elimination of measles, rubella and congenital rubella syndrome and control of mumps. MMWR 1998; 47: Wolfson LJ, Strebel PM, Marta Gacic-Dobo BS, et al. Has the 2005 measles mortality reduction goal been achieved? A natural history modeling study. Lancet 2007; 369: CDC. Progress toward measles elimination Eastern Mediterranean region. MMWR 1999; 48: World Health Organization. Progress towards reducing measles mortality and eliminating measles, WHO Eastern Mediterranean Region, Wkly Epidemiol Rec 2008; 83: Alla A, Liffick S, Newton B, Elaouad R, Rota P, Bellini W. Genetic analysis of measles viruses isolated in Morocco. J Med Virol 2002; 68: Djebbi A, Bahri O, Mokhtariazad T, et al. Identification of measles virus genotypes from recent outbreaks in countries from the Eastern Mediterranean Region. J Clin Virol 2005; 34: Alla A, Waku-Kouomou D, Benjouad A, Elaouad R, Wild TF. Rapid diversification of measles virus genotypes circulating in Morocco during epidemics. J Med Virol 2006; 78: S298 d JID 2011:204 (Suppl 1) d Naouri et al

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